Cadagno trait-based. Single-cell trait diversity in aquatic microbial communities emerges from niche and fitness differences

A fundamental question in ecology is how biodiversity is maintained and affects ecosystem functioning. Until now, it has been especially difficult to study niche and fitness differences based on single-cell traits in natural microbial communities, however, they are important drivers of biogeochemical ecosystem functions. Here we developed a new approach that defines and measures biodiversity in complex lake microbial communities (Lake Cadagno, Switzerland) based on the variation in multiple functionally relevant phenotypic traits. In our approach we use isotope probing linked to correlative imaging with confocal laser scanning microscopy and nanometer-scale secondary ion mass spectrometry (NanoSIMS) to obtain morphological (size), physiological (pigments) and metabolic (uptake of C and N isotopes and sulfur content) traits for a large number of individual cells along an environmental gradient. We show that trait evenness and divergence correlate significantly with ecosystem functioning, whereas genetic diversity measured on the level of 16S and 18S does not. Our analysis provides evidence for simultaneously increasing niche differences (measured as trait evenness in pigment composition) and decreasing fitness differences (measured as cell-to-cell variability in sulfur content) due to light limitation and competition for nutrients. This causes a negative relationship between niche and fitness differences across depth. Our results demonstrate that niche and fitness differences in microbial communities can be understood on the level of single-cell traits and that this perspective provides insights into the role of microbial communities for the functioning of entire ecosystems.